Chapter 6
Male Reproductive Strategies in Non-human Species
Copyright © 2001 Michael E. Mills
Chapter Outline
A. Male life history strategy and senesence
B. Male copulatory adaptations
1. Appetitive/impulsive sexual libido
2. Sexual indiscrimination
3. The Coolidge Effect
4. Attraction to fertile females
5. Taking risks to copulate
C. Competing with rival males
1. Fighting and bluffing
2. Coalition building
3. Social and political skills
4. Assessing rank in the male dominance hierarchy
a. Conditional strategies based on rank
5. Sperm competition
6. Sexual interference
7. Other sneaky strategies
D. Attracting and manipulating females
1. Good father behavior and commitment
2. Demonstrating health and good genes
3. Demonstrating resource control and defense
4. Deception
5. Forced copulation
II. Strategies to assure paternity
A. Assessing female sexual fidelity
B. Mate guarding
C. Infanticide
D. Sperm plugs
III. Paternal investment
Closing comments
As we have seen in the previous chapter, females have a unique set of reproductive constraints and opportunities. We explored some of the evolved adaptations designed to help maximize female reproductive success. Males have their own unique, and different, set of reproductive constraints and opportunities.
What types of problems must males generally solve to successfully reproduce? Imagine that your task is to solve male problems. Given what we've learned about females in the last chapter, how would you convince "choosy" females to select you as a mating partner? What strategies might you use to out-maneuver rival males who are competing with you for access to the most fertile females, or for the resources that females desire? If you are investing in offspring, what steps might you take to try to insure your genetic paternity? Below we will explore some of the solutions that have evolved in a variety of non-human species to solve male reproductive problems.
Male reproductive success is almost linearly related to the number of fertile females to which a male can gain sexual access. The biologist Michael Ghiselin has aptly labeled this element of the male reproductive strategy "the male copulatory imperative." Compared to females, males generally invest more in "mating effort" than in "parental effort" (Trivers, 1972). This has many effects on males -- one of which is the fact that males generally age faster than do females.
Have you ever wondered why different species have lifespans of different lengths? For example, why do humans live longer than do dogs, and why do dogs live longer than do mice? Clearly, different species senesce (age) at different rates. The theory most accepted by evolutionary biologists is that different species make different investment trade-offs between (a) somatic maintenance (repairing their bodies) and, (b) reproductive effort (producing offspring) (Nesse & Williams, 1994).
One form of somatic maintenance is DNA repair. DNA can be damaged by ultraviolet light (and other forms of radiation) and by the chemical byproducts of normal cell metabolism. In one day alone, a single human cell can accumulate 500 points of damage along its DNA strand. Cells must constantly invest energy in repairing damaged DNA by using several "repair enzymes" that find and fix most of the damage. The rate of DNA repair for a species is closely related to is lifespan (see Figure #).
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Insert Figure #
DNA Repair Rate and Senescence
(adapted from Gould & Gould, 1989, p. 24)
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Species with brief lifespans are generally r-selected: they invest relatively little effort in maintaining and repairing their own bodies. Instead, they direct their energies to reproduce as fast as they can before they die. Longer-lived, K-selected species generally invest more in somatic self-repair -- primarily to live long enough to see their offspring to independence.
Earlier we learned that males are generally more r-selected than are females. Given this, which of the two sexes would you predict
would have a shorter average lifespan? According to the r-K theory of senescence, males should generally die earlier because they are more r-selected. Compared to females, the life history of males budgets more to mating effort than to their own somatic (body) repair. In most species, it is typically the case that there are more males born than females -- that is, the sex ratio is "male biased." This bias does not last long. Throughout the lifespan, males die off at a faster rate than do females -- both from disease (due to less somatic repair) and injuries (due to male greater risk-taking or male-male fighting) (Alexander, 1987). Fisher (1930) theorized that the male-biased sex ratio at birth compensates for subsequent higher male mortality.
For example, consider a male that could out-compete his rivals by investing more energy to grow larger and more aggressive (at the expense, of course, of investing less in somatic repair). He may live a shorter life than his rivals, but he also may be more reproductively fit. For example, male
Such male-male contests are often intense. Compared to females, male red deer suffer twice the mortality (Robinette, Gashwiler, Low & Jones, 1957), due either directly to wounds inflicted during fights, or indirectly due to their weakened physical state after the rut (breeding season) when winter sets in. However, the winning male has greater access to females and, consequently, he enjoys higher reproductive success. The cost for both male winners (and losers) comes when there is little remaining somatic energy in reserve to stave of the winter cold or to survive periods when there is little food.
Males should evolve shorter lifespans as long as the benefits of investing in mating effort are enough to outweigh the costs of giving short-shift to their own body maintenance. For a human example, imagine a male gang member who impregnates five women, but dies at the age of 19 in a gunfight. Who is more reproductively "fit" -- the gang member or a more pacifist man who lives to the ripe age of 80, but only sired two children? As we discussed in earlier chapters, evolution is blind to moral considerations -- it can only "see" reproductive success. By this calculus, the violent gang member is more "fit" than is an octogenarian pacifist.
Across species, the metabolic rates of males tend to be higher than the more conservative metabolism of females. In humans, a boy's metabolic rate is 5% higher than that of a female his own age -- and this sex difference persists throughout life (Trivers, 1985). Males may literally "burn themselves out" faster than females. The greater the intensity of male-male competition, the faster we should expect males to senesce compared to females. As seen in an experiment with fruit flies, Drosophila melanogaster, males that were exposed to virgin females, literally did “burn themselves out.” In comparison with males that were exposed to inseminated females, the males exposed to the virgin females decreased their longevity while increasing their rates of courtship, mating, and sperm production in order to successfully reproduce (Cordts & Partridge, 1996).
Relative to their female conspecifics, males of more polygynous species (with more intense male-male competition) should generally senesce faster than males of more monogamous species. The hypothesis that humans have a somewhat polygynist past is suggested by the fact that human males die earlier than do women in all societies (Gosen, 1996; Smith, 1989). As we shall learn, males who are low in status, especially those who face a risk of total reproductive disenfranchisement, should be particularly willing to take risks that may jeopardize their lives in order to reproduce -- and they do (Daly & Wilson, date).
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Insert Figure # here
Ratios of women to men living at various ages in the
(adapted from Smith, 1989, p. 8)
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Insert Figure # here
Remaining years of life expectancy in
(adapted from Gosden, 1996, p. 77)
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Given that male reproductive success is typically a function of the number of copulations he can secure with different fertile females, we might expect that males with a low threshold for sexual arousal, and a high sexual libido, would generally reproduce more than sexually disinterested males. In Chapter 2, we noted Weinrich's theory that, compared to females, male libido is more "appetitive" and "impulsive" (rather than "responsive"). In many species (although there are exceptions), a male who waited for a female to initiate copulation him (rather than vice versa) would likely be waiting a long time.
Some creative researchers have tested the limits of the sexual indiscrimination of male turkeys. They found that some males will not only court a stuffed turkey, they will respond with full courtship behavior even when the head of a stuffed female turkey is removed and is suspended 15 inches above the ground. They also respond to beakless or eyeless female models (reported in Trivers, 1985). You may be familiar with a few male dogs that have inappropriately directed their mating effort to your leg -- clearly the wrong choice of species.
Why are males so sexually indiscriminant and eager? As we have seen, for females, especially mammalian females, the cost of a "bad" mating can be high. But it is generally a very different situation for males. An inappropriate mating may cost a male little -- a small amount of quickly replenishable sperm and a bit of his time. Nor will this loss generally close off other possible future reproductive opportunities with additional females. As we discussed in Chapter 4, the male minimum possible reproductive investment is generally much less than the female minimum. Males can afford to "think with their genitals" -- the costs for doing so can be insignificant. Better to make a mistake and attempt a mating with an inappropriate object (that might possibly be a female) than to allow a potential reproductive opportunity to pass by.
The exception to this general rule is the sexual behavior of males of species that are obligated to invest parentally (such as many bird species), or where males present females with a costly "nuptial gift." The greater the male obligatory investment in courtship or parenting, the more sexually choosy, and discriminating, males become. As you might predict, the male tendency to mate indiscriminately decreases as the costs of an inappropriate mating increase. However, when choosing between two or more females at one time, males generally make choices that make reproductive sense. There are two important characteristics by which males do discriminate between females. Males mate preferentially with females that evidence signs of fertility, and females with which a male has not recently copulated. We will discuss both of these considerations below.
Imagine a cattle rancher who has bull in a pen. If a female is placed in the pen, the bull will likely copulate with her once, perhaps a few times, and then he will stop. However, if that cow is replaced with a new cow, he will copulate with her, too. If we did an experiment and, all day long, continued to provide the bull with new cows, how long do you think he would continue to copulate? Answer: virtually all day long (Beamer, Bermant & Glegg, 1969; Dewsbury, 1981; Schein & Hale, 1965). Actually, he will copulate to the point of exhaustion (which, for bulls, is about 60 - 80 times). Why, if the bull was so libidinous that he desired to copulate all day, did he stop copulating with the first female?
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Figure #
Insert diagram from Beamer, Berman & Cleg, 1969
The Coolidge Effect in Sheep
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By now you should anticipate the answer. Each new cow represents a new reproductive opportunity to the bull.
Additional copulations with the first cow would not much increase the likelihood of impregnating her -- one or two copulations will usually suffice. If he copulates ten times with one cow he will, at most, impregnate one cow. But if he copulates one time with ten different cows, ten pregnancies may result. This phenomenon of male re-arousal by a sexually novel female has been termed the "Coolidge Effect" (Bermant, 1976). The term is derived from a real event (based on a rather humorous comment made by the former U.S. President Coolidge -- but we will save that anecdote for Chapter 9).
For now, back to the bull. That sexual novelty is the salient factor here is illustrated by the fact that a bull remains disinterested even if the original cow is removed, then re-introduced to him later the same day. However, if the cow is introduced to a second bull,
she is sexually novel to him, and we can predict his response. Animal behavior researchers investigating the Coolidge Effect have attempted to fool males by covering the heads of females with sacks or by applying smelly substances to mask the scent of the female -- all to no avail (Beamer et al., 1969; Bermant, 1976). Despite the efforts of the researchers, the males could discriminate between sexually familiar and novel females. This certainly makes sense -- if males did not have an ability to recognize individual females, they could not have evolved an interest in preferring sexually novel ones (Symons, 1979).
The Coolidge Effect is a pan-mammalian phenomenon. However, its intensity varies in different species. Males of species that have predominantly monogamous mating systems show a less intense Coolidge Effect than do males of more polygynous species (Bermant, 1976). This is likely because males in monogamous species have fewer opportunities to mate with sexually novel partners. However, when the opportunity for an extra-pair copulation arises, many putatively monogamous males take advantage of it, especially when their mate is not looking. Studies of several bird species have found that males were more likely to pursue extra-pair copulations when their mate was unable to observe them (Baltz & Clark, 1997; Beecher & Beecher, 1979).
Males of all species should be selected to find fertile females the most sexually attractive. In most species, females are not sexually receptive until they are close to the time of their ovulation. Male primates, with the exceptions of humans and male bonobo chimpanzees, are generally far less interested in females who are not in estrous. Human males, however, have a particular problem in this regard -- they can't tell when human females are ovulating! We will explore the reasons for concealed ovulation in women, and its consequences, in later chapters.
Since the number of available, sexually receptive females
limits male reproductive output, males should actively search them out. They do. Male ground squirrels use information about a female’s reproductive state and habitat location to seek out females in estrus at times with the most potential for success (Schwagmeyer, 1995). One way that male insects search to find females of their own species is by their scent. The females release an attractive pheromone that the males use as a homing device to find females (Landolt & Heath, 1990).
About a dozen of the 12,000 species of butterflies have been studied and show the importance of both color and odor in mate selection. Butterflies use color to help determine the sex of a potential mate. For instance, the Little Yellow butterfly, Eurema lisa, appears identical yellow to the human eye regardless of sex. However males look different to females who perceive light at wavelengths in the ultraviolent spectrum, invisible to the human eye (Rutowski, 1998). The yellow wing scales of males reflect ultraviolet light and thus attract females while female wings do not (Rutowski, 1998). When males age, the ultraviolet light becomes less and less reflective, thus attracting fewer and fewer females, signaling the decreasing fertility of the individual male. Besides color, pheromones are used as indicators for mate selection and identification. A male deposits pheromones from his antennae onto a potential mate, which serves as a chemical signal telling the female to remain still while the male copulates with her (Rutowski, 1998).
For some species of fish, searching for, and retaining, a mate in the open ocean can present a particular challenge. The males of a species of anglerfish solve this problem in a rather spectacular way (Gould, 1982). Once a male finds a female, he bites into her flank and literally burros his way into her body. Eventually his body own shrinks and it becomes incorporated in hers. His testes, however, enlarge and they are put in service of fertilizing her eggs. The sexual dimorphism of this species is extreme -- males are two inches long, female length is 26 inches. Males of this species are not designed to fight with other males -- their bodies are designed to simply be sperm delivery torpedoes.
In their search for mates, males generally disperse more widely than do females. This tendency for greater male geographic mobility has been documented in a variety of species including turtles, snakes, salamanders and mammals (Trivers, 1985).
Males also call out to solicit a mate. As we shall see, whenever there is a loud commotion in nature, it is often the males who are making the racket, from the roaring of lions, the territorial songs of birds, the croaking of toads, to the trumpeting of bull elk. Males are calling to attract females, as well as to let other males know that the territory is occupied.
The male copulatory imperative is so intense in some species that males may be willing to risk their lives to copulate. During copulation, the female mantis may turn around and consume her mate's head. No matter -- his headless body can continue to copulate for up to 20 minutes! The male copulatory imperative evidently is so strong that in some species males have evolved the physical and neurological mechanisms to copulate even without a brain.
Males are also willing to risk getting eaten by predators (other than their mates). Male Saharan gerbils must risk predation when they
travel to visit females for a chance to male. The females are relatively secure in their own territories, which they select based on the availability of food resources. The males must frequently leave their own territories to make the rounds of females who are infrequently ready to mate. The male gerbil mortality is higher than it is for females -- often resulting in highly female-biased sex ratios (Daly & Daly, 1974).
Male wolf spiders face similar threats of predation in order to mate. Females prefer males with have a high drumming rate, a characteristic of wolf spider courtship. This high drumming rate is not only energetically costly but also attracts predators (Kotiaho et al., 1998). In fact, 13.3 % of the predated males studied were caught immediately after drumming occurred. Similarly, as with male drumming, mate-searching is an activity beneficial to males in finding mates but also one that it highly costly due to the increased risk of predation while doing these activities. Wolf spider males must maximize these beneficial behaviors while minimizing the costs and risks associated with them, including energetic costs and predation (Kotiaho et al, 1998).
As we have learned, females represent a limited reproductive resource to males. Consequently males generally compete more intensely for sexual access to females than vice versa. This is particularly evident in many species during the breeding season. For instance, fallow bucks that gained matings with females had higher rates of fighting than fallow bucks that did not gain access (McElligott & Hayden, 2000). Winning contests with other males provides a benefit beyond access to females: the females themselves generally prefer to mate with winners. And, as well shall see, at times the competition for females can turn quite violent.
In groups of primates consisting of a large number of females and only one male, as is the case with polygynous maqaque or baboon groups, the resident males must compete with outsiders for the chance to mate. Females of these species remain in their natal group throughout sexual maturity, but males emigrate as they mature (Pusey & Packer, 1987). Young emigrating males are forced then to either conquer an existing group by ousting the existing male, or find females to start a new one-male unit on his own.
When the sex ratio is male-biased (more available males than available females), the fighting is often much more intense (Souroukis & Cade, 1993). But a male may not always have to defeat rivals in direct fights -- sometimes intimidation alone, or bluffing, will suffice. In species that do have direct, physical contests, males are often physically larger, stronger, and are more ferocious than females. As we shall see, in several species males have literally evolved morphological weapons with which to fight.
Males prepare early in life for male-male competition. In most species, juvenile males engage in more vigorous "rough and tumble" play than do females. This behavior includes chasing and play-fighting. The putative function of such play behavior is to give young males the experience to learn complex and rapid motor skills needed to engage in real intra-sexual contests later in life (Symons, 1978).
Females generally are the "right" size, shape and coloration to survive in their ecology. When males deviate from the female "optimum" -- with bright colors, size dimorphism, or with structures that females lack -- such deviations are generally due to sexual selection. In a controlled experiment of sexual selection in lekking cichlid fish, female fish were influenced in choosing a mate by male behaviors and characteristics, most specifically his size. Female selection and male-male competition/interactions played a significant role in the sexual selection strategies of this fish species (Nelson, 1995). Male size was also a factor in sexual selection of smallmouth bass fish. In an experiment by Wiegmann and Bayliss (1995), it was predicted that due to the dependence of metabolic rate on body size, larger males can provide a greater investment in offspring than smaller sized males; thus, strengthening the female tendency to choose large males as mating partners.
Unique male morphology has also evolved independently of female preference in several species to help males win battles against their rivals, including enlarged canine teeth, tusks, horns, antlers, pinchers, etc.
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Insert Figure # about here
Weapons in male beetles
(Cyclommatus imperator)
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The antlers of some male mammals are enormous. Their size and weight are a significant burden to males -- they can become impediments when they get entangled in bushes or trees, and the added weight makes escaping from wolves more exhausting. Like most male morphological weapons, male sex hormones cause their development. Castrated moose, for example, do not grow antlers.
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Insert Figure # about here
Antlers as male weapons
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In some species, males also grow defensive physical characteristics that the females lack. The mane of the lion is not designed to charm lionesses -- it is a defensive device to protect their necks from lethal "go for the throat" attacks of other lions (Gould & Gould, 1989).
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Insert Figure # about here
The mane of a lion.
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When males fight, larger males are more likely to win. Larger males, such as in the southern elephant seal, also have a higher likelihood of high reproductive success (Modig, 1996). This produces directional intraspecies selection pressure with respect to male size. As a consequence, there is more sexual dimorphism (e.g., males larger than females) in species in which males fight (e.g., Alcock & Houston, 1996). For example, a study of lizards found that the largest males monopolized 84% of the matings and fertilized 88% of the eggs (Censky, 1995). This effect also is apparent in primates and ungulates (antelopes and deer). Generally, the more polygynous the species, the larger the male is compared to the female. For example, in
There are exceptions to the general rule of intra-sexual sexual dimorphism. For example, in certain frog species the breeding season is so short, and so many females are available simultaneously, there is little advantage to being a large male. The monogamous South American night monkey is about the same size as the female. Male snakes are typically smaller than their female counterparts. However, this dimorphism is reversed in snake species in which males fight for access to females (Trivers, 1985).
The term "aggressive" does not always mean "violent." The costs of fighting can be very high: the energy consumed, the risk of injury, and, in some species, the risk of death. If males can "size each other up" and accurately assess who would be the likely winner if it came to a fight, they can decide who wins based on "points" rather than in a dangerous altercation. For example, the antlers of
Male elephant seals show extreme size dimorphism, and thus we might predict that the contests are particularly violent. The bulls rear up and butt chests and heads, biting each other's neck and body. But, as noted earlier, access to females is only part of the equation. The females themselves generally prefer the winners of contests. Therefore, the largest males and those with the large harem size have the greatest mating success (Modig, 1996). When a subordinate male elephant seal sneaks up onto the beach and attempts to copulate with a female, she will bellow to alert the dominant male of the intrusion. Thus, female choice augments the intra-sexual selection pressure on males for increased strength and size.
Even male animals that have not evolved combat weapons can fight violently.
The most timid animals, not provided with any special weapon for fighting, engage in desperate conflicts during the season of love. Two hares have been seen to fight together until one was killed; male moles often fight, and sometimes with fatal results; male squirrels engage in frequent contests, and often wound each other severely; as do male beavers, so that hardly a skin is without scars.... It is notorious how desperately male seals fight, both with their teeth and claws, during the breeding season.... The courage and desperate conflicts of stags have often been described; their skeletons have been found in various parts of the world with the horns inextricably locked together, showing how miserably the victor and vanquished had perished.
It is often in a female's interest to select the winner of male-male competitions. In one sense, the females are making the males do their work for them -- rank ordering the males with the best genes and health (Cox & Le Boeuf, 1977). However, sometimes females do not simply accept the winners of male-male contests -- in some species they use additional criteria for evaluating males. As we shall explore in more detail later, females may evaluate males by their displays, which also consume energy (Gibson & Bradbury, 1985; Krebs & Harvey, 1988). Of course, this puts additional burdens on males -- no wonder they generally do not live as long as females!
In some cases it makes sense for a male to form coalitions with other males to compete more effectively. The individuals involved must surrender their possible dictatorship among the group, but are more comfortable in their coalition with allies. A good example of male alliances is found in lions (Packer & Pusey, 1997). Male lions must take over a pride (a group of breeding females) to reproduce. This is not an easy task because prides are protected by one or more resident males. Often, only by joining forces with another lion (sometimes his brother), does a solitary lion have much hope of a successful pride take-over.
Franz de Waal (1982) recounted an interesting example of the power of coalitions among male chimpanzees. The dominant, or "alpha," male, which the researchers named "Yeroen," translated his high status into reproductive success. When females came into estrous, Yeroen monopolized 75% of the matings. Yeroen's dominance remained unchallenged until advancing age began to take a toll on him. Eventually he was challenged and ousted by a younger male, Luit. Yeroen was subsequently denied sexual access to all estrous females. That might have been the end of the story (and it usually is), however, Yeroen had one last trump card to play. Yeroen had developed a friendship with a young male named Nikki. Although neither of them dared challenge Luit's dominance alone, together they formed a coalition against Luit. The fights that ensued were bloody, but their coup was successful. Thereafter, 50% of the matings went to Nikki, while the once-ousted Yeroen managed to secure 25% of the matings. Male reproductive coalitions are also found in several other species, including dolphins (Connor, Smolker, & Richards, 1992) and baboons (Hall & DeVore, 1965).
Chimpanzees such as Yeroen develop long-term, stable relationships with their allies. However, not all alliances are this unwavering. Baboons, for instance, secure quick, transient alliances with other males only to increase mating success for short periods of estrous in females. These types of coalitions can be more harmful, introducing new males to the alpha male alliance and sometimes result in severe injury to the ousted individual (DeWaal, 1982, 1986, 1992).
As the story about Yeroen suggests, among social species political and social strategies can factor in a male's reproductive success. Female olive baboons often select as mating partners those males with whom she has developed a "friendship" -- even if he is not among the top ranked in the male hierarchy (Smuts, date; Strum, date). These are the males who may be depended on as protectors and allies in times of need.
In species in which males form dominance hierarchies, each male knows his relative status and generally behaves deferentially to those above him, while he intimidates those below. Dominant males advertise their status behaviorally. In rhesus monkeys, alpha males keep their head and tail up and move about in an unhesitating and deliberate manner. You may be familiar with the behavior of dominant dogs, which also hold their tails up as a sign of dominance. A subordinate dog will literally tuck his tail between his legs.
In chimpanzees, high rank has its perks: access to the best sleeping and feeding size, and preferential (although, in this species, often not exclusive) mating access to females. One researcher examined the relationship between dominance rank and reproductive success over a 15-year period in male rhesus monkeys (Smith, 1993). As expected, the highest ranked males secured the most copulations. Fallow bucks that gained access to females possessed a high social dominance rank compared to fallow bucks that were unsuccessful in mating with females (McElligott & Hayden, 2000). Cowlishaw and Dunbar (1991) concluded, through a comparative analysis of the relationship between rank in a group and mating success in 75 groups of 14 arthropods, that there is a positive correlation between a male’s dominance and his frequency of mating.
As we have seen, brute strength is not the only factor in determining dominance -- cunning and ingenuity figure in as well.
Jane Goodall (1971) witnessed an incident in which a subordinate male promoted himself to alpha rank without a physical fight. He did this by banging two empty kerosene cans together as he ran down a hill toward the dominant males. They were so frightened by the noise that they forfeited the bananas that they were eating, as well as their high status.
Subordinate males generally have lower levels of testosterone
(see, for example, Barnard, Behnke & Sewell, 1996) -- a result of what is sometimes termed "psychological castration." When social rank declines, both testosterone levels and immunocompetence decline as well. Testosterone is believed to “enhance motivational aspects of mammalian sexual behavior” (Alexander et al, 1994). With declining levels of testosterone, subordinate rank is acknowledged by males as they assume the female role in copulation (Trivers, 1976). For example, among mountain sheep, the victor often mounts the loser when the fight ends (Geist, 1971). The “psychological castration” effect was also documented in a study of male mice. Their rank was lowered experimentally by isolating them and exposing them to the scents of unfamiliar males (Smith, Barnard & Behnke, 1996).
This “psychological castration” effect can be evident not only in sexual situations, but also in normal social situations. Once an animal has been subordinated and its level of testosterone decreased, its level of aggression lowers as well. Studies on talapoins show that the low-ranking animals glance more often at the high-ranking animals than vice-versa. These observations correlate with dominance in situations involving aggression (Keverne, et al., 1978). A definite hierarchy also occurred among six males (three adults and three sub-adults) in a semi-free-ranging heterosexual group in the case of the mandrill. Outside the group, three other adults lived a semi-solitary life. Rate of copulation was correlated with dominance rank, and in this case the alpha, group associated male had 70% of all ejaculations. The alpha semi-solitary male accounted for 7% of the ejaculations, and the sub-adults had almost no ejaculations (Bercovitch, 1986: Mcmillan, 1989). In another study of a group consisting of 18 adult male stumptail macaques, 87% of the matings were by the 4 highest ranked individuals (Nieuwenhuijsen et al., 1987)
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Male rank and copulatory frequency
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Males may adjust their competitive tactics facultatively, conditional on their rank. Among chimpanzees, dominant males attempt to monopolize matings with estrous females.
Less dominant males may attempt to lure a female to leave the group, consort with him for several days, and copulate as an exclusive pair. When no clear dominant male emerges, chimpanzee males may mate opportunistically with any estrous females (Tutin, 1979). As noted earlier, subordinate baboons develop "friendships" with particular females. Like chimpanzees, they consort with their female "friends" and attempt to remove them from close proximity of dominant males (Packer, 1979).
In his book "Chimpanzee Politics: Power and Sex Among the Apes," Frans de Waal (1982) recounted another incident in the series of contests between Luit and Nikki. When Nikki was dominant, he caught Luit making sexual advances toward a female. Nikki immediately rose to his feet and slowly moved toward Luit, picking up a rock along the way. Once Luit caught sight of Nikki, his demeanor changed. Although he was sexually aroused, Luit moved a few feet away from the female. He carefully sat down with his back toward the advancing Nikki. Luit had something to hide -- an erection. He looked back and forth between the advancing Nikki and down at his penis, which was slowly deflating. When his penis was no longer visible, Luit finally rose up and submissively approached Nikki. He nonchalantly inspected the stone that Nikki was carrying, and he then walked past him, leaving Nikki with the receptive female.
In social conditions characterized by instability as mentioned above, aggressive males tend to demonstrate elevated testosterone levels, necessary to assert their dominance (Dixson, 1998; Sapolsky, 1993). During these periods of instability, subordinate males show a decrease in testosterone. On the other hand, the levels of circulating plasma testosterone do not predict sexual arousal or copulatory activity within male primates as long as enough hormone is present to maintain sexual behavior (Dixson, 1998).
Subordinate males who make such mating attempts behind the back of the alpha male are known as "sneaky copulators." If the female is not receptive to these advances they may notify the dominant male of the situation. For example, pre-adult elephant seal males are still small enough to be mistaken for a female. These subordinate males often attempt to sneak up on a beach controlled by the harem holder and furtively copulate with a female.
As noted earlier, the females are often not impressed and vocalize to attract the attention of the dominant bull.
Once the interloper is discovered, the alpha male promptly
escorts the subordinate male off the beach.
When males cannot prevent other males from copulating with
their mate(s), another form of competition evolves: males
literally compete with their sperm. Imagine that two chimpanzee
males that have both recently copulated with the same female. If the female conceives that day, what is the probability that the first male is the father the resulting infant? If we assume that both males produce equal quantities of viable sperm, the first male has a 50% chance of being the father. However, imagine that the second male produces twice as much sperm as does the first. The second male would now have a 66% chance of being the father; the chances of the first male would drop to 33%. Sometimes it is the male with the most sperm who wins.
In another primate species, the macaques, there is little sexual dimorphism; therefore, there is a slight chance that a male will be able to monopolize a female. Instead there is often a scramble for mating opportunities in macaques; thus, higher levels of sperm competition are observed to increase a male’s opportunity to reproduce successfully (Dunbar & Cowlishaw, 1992). As expected, due to several males mating with a single female, mating is an insufficient predilection of paternity. In fact, in black bears that were tested for paternity using DNA fingerprinting, it was demonstrated that within a litter, it is possible to have more than one father of the offspring (Schenk and Kovacs, 1995). The results of the DNA fingerprinting showed that multiple matings was practiced by both sexes, which increased the importance for a male of sperm competition (Schenk and Kovacs, 1995).
In a certain species of birds called dunnocks, males have a particular problem -- sometimes the females are polyandrous (have more than one mate at a time). Males of this species thus must also compete with their sperm. They copulate frequently as a method of "damage control" when indications of infidelity are present (Birkhead, 1988; Smith, 1984). In addition, they will peck at the female's cloaca (reproductive tract) until she expels any sperm from previous matings (Davies, 1983).
Other sperm competition adaptations are wonderfully intriguing. The penis of damselflies has barbs on it designed to remove any sperm from competitors that may already be in the female reproductive tract (Waage, 1979). Male fruit flies have a protein in their sperm that causes females to produce more eggs (Rice, 1996). A male honeybee sacrifices himself -- his body explodes like a grenade to drive his sperm into the female reproductive tract (Barash & Lipton, 1997). Male bedbugs inject their sperm into competing males -- who then transfer it into other females (Lloyd, 1979).
Reproductive success is relative -- relative to the success of one's competitors. It can be increased both by (a) increasing one's own reproductive output, as well as (b) decreasing the reproductive success of same-sex competitors. The latter type of outcome may be realized by what is called "sexual interference."
Male salamanders compete to have their spermatophores (sperm containing sacks) picked up by a female, who then places it in her reproductive tract. The game in this species becomes one of "who can top who." An interfering male may place his spermatophores on top of the one left by the first male. The first male may then put his second spermatophore on top of the interloper's, and so on (Barash, 1982). This can be called the sexual-competition hypothesis, the reduction of mating success by a harasser (Neimeyer & Chamove, 1983) or the attempt to gain a sexual partner at the expense of one of the current mating individuals (Hall, 1965; Loy and Loy, 1977).
Some species of grasshoppers introduce "
Polygamous male birds have decreased broods relative to monogamous males because of sperm competition (Moller and Ninni, 1998). For example, male bowerbirds collect colorful objects that they place near their bowers to attract females. Rather than finding their own colorful items, dominant males raid the bowers of other males, perhaps both increasing their likelihood of attracting a female, as well as decreasing the desirability of the rival's bower.
Members of over 30 primate species - including ringtailed lemurs, squirrel monkeys, langurs, macaques, baboons, chimpanzees, and bonobos - have been studied interrupting or harrassing copulations of conspecifics (Neimeyer and Anderson, 1983). Harassment is equivalent to a lesser form of interference, such as touching or slapping. This behavior rarely results in interruption; the copulating male usually ejaculates in these situations.
Hierarchy plays a role in whether a male can interfere in copulation. For example, Figan was the most successful chimpanzee in his community. Over a two-month span, Figan successfully interrupted copulation by the lower-ranking males, but was never interrupted by the lower ranking chimpanzees. The same observations were made when observing alpha male stumptales. Bruce and Estep (1992) observed 829 copulations by alpha males. Although they were harassed many times by both other adult females and sub-adult, there was never an attempt by one of the other animals in their group to interfere. In the same study, the alpha males interrupted 33% of the beta male’s copulations and 39% of copulations involving younger males.
In some species, inhibition costs, which increase with the size of the subordinate male, play an important factor in a dominant males level of aggression during interference. If the costs “outweigh” the benefits, the dominant animal will cease interruption of copulation. This was shown using alpine marmots, where the dominant male always attempted to inhibit reproduction by an inferior male, but varied in its aggression according to the size of the competition (Arnold and Dittami, 1997).
In some species, males do not even have to wait for the female to give birth to an offspring sired by another male before committing infanticide -- their scent alone can cause the abortion of the fetus. This phenomenon, called "the Bruce Effect" (after its discoverer, Hilda Bruce) occurs when a pregnant mouse smells the scent of a new male.
The creativity of male strategies can be astounding. Subordinate "satellite" frogs wait silently near larger, croaking frogs and grasp any female that comes by attracted by the croaking (ref). Similar behavior is found in male crickets. The advantage to silent "satellite" males is that they avoid predators attracted by the noisy mate calling. They also avoid the energy expenditure of defending a territory. The cost/benefit trade-offs between the two strategies (caller and satellite) can fluctuate over time (e.g., as a function of the number of nearby predators), such that "frequency dependent" selection operates to vary the ratio of the two types of males.
Sometimes the strategy chosen is not obligatory --males can switch their strategy -- for example, a silent satellite decides to engage in mating calls -- depending on local conditions. Among crickets, callers and satellites are the same size, so they may decide to switch strategies on successive nights. One reason why they may switch is to conserve energy -- calling can be exhausting!
When different strategies are genetically fixed, males may evolve into different physical or behavioral "morphs." Small male sunfish mimic female behavior so well that they are allowed into the nesting site of the dominant male -- where the "transvestite" sheds his sperm on the eggs previously deposited by females. Salmon have three different male morphs: (a) those who go out to sea for several years before returning to their natal stream to mate, (b) "jacks" who return after only a year at sea, and (c) "precocious parr" who never leave the stream. Compared to the full-grown male salmon, parr are tiny. The jacks are intermediate in size between the two other male morphs. Both jacks and parr interlope near the spawning full-size male and his mate, and, at the crucial moment, attempt to release their sperm before the larger male attacks them. Because humans fish for the full size salmon, the benefits of being a "sneaky" male have been so great that some streams have few full-sized males left. The large size male salmon morph may eventually go extinct. In another species of fish, less influenced by human fishing preferences, there are also three distinct male morphs, but each have been found to have equal levels of mating success (Shuster & Wade, 1991).
In some species, males copulate for long periods of time (far longer than is needed for sperm transfer), or mate repeatedly, thus preventing other males from copulating with a female. Insects called "love bugs" are aptly named. To prevent other males from copulating with his mate, a male will retain his copulatory embrace for up to three days (Thornhill & Alcock, 1983). Copulation can last up to one week in one species of butterflies (Labitte, 1919, reported in Parker, 1984). Males also copulate with greater frequency to assure their paternity (Briskie, 1992; Simmons, 1990). Higher copulatory frequencies are observed more often in polygynous than in monogamous species of primates (Dixson, 1995).
To convince a female to copulate, males have two basic strategies: honest and dishonest. Honest strategies offer something of value to a female that will likely increase her reproductive success (e.g., good genes, resources, protection, etc.). "Dishonest" strategies involve deception, or even outright force. The purpose of both of these strategies is to induce a female to copulate by offering her resources that she wants.
As we have seen, males do a variety of things to attract females, from the croaking of frogs, the light shows of fireflies, to the intricate songs of birds. It is clear that these "broadcast displays" are designed to attract females because they often stop immediately after mating (Kendeigh, 1945). The advertising restarts when the male is ready to find another mate, or if the show is also designed to inform other males that the territory is occupied. Manipulating their “broadcast displays,” fallow bucks that are successful in mating show increased investment in vocal display during the mating season than unsuccessful males (McElligott & Hayden, 2000).
Sometimes males engage in joint advertising to increase the intensity of the signal so that females even some distance away will be attracted -- such as the impressive joint light shows of fireflies and the conspicuous auditory and visual exhibitions of males that group together to form a "lek." A lek is a meeting place -- a place where males congregate for the purpose of attracting females and allowing the females to check out their displays -- perhaps something akin a human dance club.
In
The causes of female preferences for particular male colors, shapes, smells, or behavioral displays is easy to understand if they are honest signs of greater male genetic fitness. In the insect, Drosophila
As in Drosophila
Or, it may be that males are exploiting a feature that females have good adaptive reasons to prefer. If it is adaptive for penhens to evaluate male eyes, the peacock can exploit that preference with many colorful eye-like spots on his tail (Ridley, 1981). Male satin bowerbirds have blue eyes -- perhaps this is why they decorate their bowers only with blue objects. These would be examples of "super-normal" signals -- exaggerations of traits that, to females, have been good indications of male genetic quality. Female preferences may thus be guided by male competition that serves to amplify the male traits that females originally preferred. Males may be attempting to fool females with super-normal signals. We might anticipate a spiraling evolutionary arms race between the male exploiting super-normal traits and females trying to discern true markers of genetic quality.
In K-selected species, raising offspring is often an arduous task. Females should prefer males willing to assist with feeding, sheltering, and protecting offspring. In many species males are either unable or unwilling to do so. However, in those species in which males can help, and given that the males have some assurance of paternity, male parental investment can be a highly prized resource to females. However, not all males are equally good fathers, so females should attempt to evaluate likely male parental investment before mating. This gives males yet another test to pass before they are allowed sexual access to a female: what we might term the "good father behavior" test. How can males demonstrate good fathering behavior?
One way is to offer females food during courtship -- demonstrating both their ability to acquire it and their willingness to share it with her, and, by implication, any future offspring. Male scorpion flies, for example, offer food to females. Females refuse to mate with a male until he has offered such a nuptial gift. Furthermore, the gift must be of a certain size -- if it is too small, she refuses both the gift and his offer to copulate. If it is of intermediate size, she will take the food but not allow copulation long enough for the male to transfer all of his sperm. Only if given a large gift does the female allow a full-length copulation (ref). Among some species of sea-faring birds, males will tempt a female by teasing to offer her a fish that he has caught. If she appears to be receptive to him, eventually he will give her the catch. Their first copulation typically follows soon thereafter. Eventually, she stops catching her own meals and relies exclusively on his generosity (Trivers, 1985).
Nest building quality is one criterion that many species of birds use to evaluate male potential parental investment. Male weaverbirds knit together elaborate hanging nests to attract females. Females do not merely visually inspect the nest; they may tug at it to assess the quality of the construction. If females reject his nest (and thus him, too), he will tear it apart and start building a new, and hopefully better, nest that can pass female assessments.
Sexual reproduction can be likened to a business partnership where two partners merge their capital with the hope of realizing a profit. Before agreeing to such a partnership, each will want to assess the quality of the resources that the other has to offer. Similarly, before reproductively merging her genes with the 50% offered by a male, a female would do well to assess the quality of those genes. Since genes cannot be directly observed, she can only make indirect assessments. Females often observe the body size and other phenotypes, courtship behavior, and aggressive success in choosing whom to partner up with (Boake and Konigsberg, 1998). Kodric-Brown (1995) conducted a study on male pupfish to determine past mating dominance on subsequent success. He found that, in pupfish, previous mating history indicates the future dominance quite well.
Males of some species advertise their genetic quality, their health, and freedom from parasites with their bodies. The intensity of redness of male stickleback fish is correlated with their genetic quality and physical condition, and females mate preferentially with males with more intense red color (Bakker & Milinski, 1993). Female houseflies also mate preferentially with colorful males (Hill, 1990).
Male genetic quality can also be assessed by the odors they emit. Female house mice preferred the odors of the sons of well-nourished females over the odors of the sons of undernourished mothers (Meikle, et al., 1995). Essentially, the odors emitted by the house mice demonstrated the health and fitness of the sons of well- and malnourished females. The diet of a male can also influence the odors he emits. Meadow voles fed a high-protein diet possessed odors that attracted females over the individuals on a low-protein diet (Ferkin, et al., 1997). The high-quality diet producing beneficial odors is a sign for a higher-quality individual, demonstrating good health.
The reproductive success of certain animals also depends on the amount of symmetry that an organism has. Fluctuating asymmetry refers to the amount of asymmetry that an organism has throughout its body. The more symmetry one has, the more attractive one will be to possible mates. Symmetrically banded male zebra finches sired more offspring than did more asymmetric males, due to female choice (Swaddle, 1996). However, when two drosphilia species with different amounts of asymmetry were studied, no differences in mating were found between animals regarding fluctuating asymmetry, although differences were found regarding other differing qualities. These observations suggest that fluctuating asymmetry has little to do with the mating success of an animal (Markow, et al., 1996). It is likely that future research will help to sort out these conflicting findings.
If a male can control resources that females want (e.g., food, water, shelter, a good nesting place) and keep other males away, he may be able to forgo searching out females -- they will come to him. For example, wood-boring bees will defend a patch of flowers from other males and will only allow a female to stay if she is willing to copulate. To certain species of female flies, a fresh cow pat (cow dung) is a valuable resource -- they lay their eggs on them. Males thus stake out the edge of the cowpat and wait for females to arrive.
What about males who do not have any of the resources that females want? They can attempt to deceive females. Males of some species of spiders offer a dead insect as a nuptial gift. But first, they wrap it with the same material that they use to construct a web. Males who have no gift to offer will sometimes still present a boxed present -- but it is empty. It requires some time for the female to open the gift, enough that the male may be able to complete copulating before she discovers his deception. Even a male who has a real gift may wrap it so thoroughly that the female cannot open it before he is finished copulating. At that time, he may take it from her and offer it to a new female (ref).
Females may evolve counter-strategies to male deception. One way is to evaluate males by traits that second-rate males cannot fake -- or that they can fake only at great cost or risk. For example, female frogs and deer prefer males with loud, deep vocalizations, sounds that, because of their size, small males cannot fake. Even if males can fake a signal, it may not always be in their interests to do so -- other males may call their bluff. Honest signals are more likely to evolve than dishonest ones because the latter will eventually be identified, devalued, and eventually ignored (Daly & Wilson, 1982).
As we have seen, courtship is a period of mutual evaluation between potential reproductive partners. Males are generally more indiscriminant and eager, leaving females the luxury of evaluating several suitors before they consent to sex. Males who are repeatedly rejected are in a reproductive quandary. They may be left with only one remaining viable option: forced copulation, or rape. “Humans are not alone in the commission of crime, except in the rather trivial sense that crimes can only be committed by ‘adult’ humans living in societies where written criminal statutes exist” (Ellis, 1998). Natural selection has made it almost rewarding to force copulation, however, for certain species in certain situations (Ellis, 1998). In the Japanese quail, forced copulations had the same fertilization success as other copulations, proving that these forced interactions can be a successful strategy for males in increasing reproductive strategy (Adkins-Regan, 1995).
Rape has been documented in a wide spectrum of species, from insects to primates. The list includes fruit flies, snow geese, bank swallows, right whales, wild dogs, gorillas, chimpanzees and orangutans. Even organized gang rape occurs in some species -- something you may have witnessed yourself if you have spent much time near ponds with mallard ducks. In this species, a group of unmated males will target a female when her mate is away. The courtship rituals common to this species are notably absent as the males chase her across the water. Once they catch her, they bite the back of her neck, and may dunk her head under water (sometimes drowning her). Several males may copulate in succession with the victim. Once her mate has managed to disperse the gang, he forcibly copulates with her himself to compete with the rapist's sperm (Barash, 1977).
Forcible copulation is also rampant in primates, particularly in bonnet maqaques (Glick, 1980). In Glick’s study, “forcible copulation by the aggressive pursuit and restraint of a screaming female, whose efforts to escape the male were unsuccessful.” In free-ranging mantled howlers, the infrequent attempts to forcibly copulate were quickly repelled by the females with bared teeth accompanied by loud screams (Jones, 1985).
Male scorpion flies without a nuptial gift to offer may attempt to collide with a female in the air -- knocking her to the ground where they then attempt forced copulation. Males of some species of songbirds use the same tactic (Birkhead, Atkin, & Molter, 1987). However, males generally prefer "honest" courtship, and only resort to forced copulation when other reproductive avenues have been closed (Thornhill, 1980, 1981).
To reproduce optimally, males must do more than simply gain sexual access to females. To whatever extent they can, they must attempt to prevent other males from copulating with their mates. Males do this to increase their reproductive output relative to other males, and, when males invest parentally, to insure their paternity. In a biological sense, a cuckolded male is squandering any investment he is making on offspring that do not carry his genes. This is, metaphorically, genetic suicide.
Males utilize two different strategies to help ensure their paternity (Trivers, 1985). One method is to guard their mate(s) from other males to prevent insemination by "alien" sperm. If that fails, the second method is to compete with sperm, as we discussed earlier.
If females were always faithful to their mates, males would have little concern about their paternity. However, as you read in the previous chapter, at times it can be in a female's interest to engage in extra-pair copulations (EPCs). In one study of red-winged blackbirds, mated males were vasectomized. Later, instead of laying infertile eggs, some the mates of these males laid eggs that produced hatchlings! These females obviously were obtaining sperm elsewhere (Bray, Kennelly, & Guarlno, 1975). A male that was cuckolded thus squandered his parental investment for an entire breeding season -- one of the few that he will have in his brief blackbird life.
In a study of reproductive strategies of flour beetles, it was observed that males preferred to copulate with virgin females over previously mated females in order to ensure their paternity (Lewis & Iannini, 1995). Unfortunately for males, the females they encounter may not all be virgins.
Before a male invests in a female and her future offspring, it would wise to insure that she is not already impregnated by a previous suitor. One purpose of a courtship period from a male perspective is to determine if his potential mate shows signs of pregnancy a little too soon. In addition, during the courtship period, males of species that invest in their own offspring should evaluate their potential partner's likely sexual fidelity. A female's prior sexual behavior, her current sexual fidelity, and the degree to which she rejects, rather than responds, to the advances of other males are likely to be assessed. A negative assessment will reduce the probability that a male will invest parentally.
In barnacle geese, a study using DNA fingerprinting was done to establish the ratio of extra-pair young, or young fathered by another male, in a particular population. Approximately 17% of the young fingerprinted were found to be extra-pair young (Larsson, Tegelstrom, & Forslund, 1995)
In one species of doves, males are wary of females who respond too quickly to their courtship displays. In this species, a female's sex hormones and her sexual receptivity are triggered by male courtship. A female who is easily aroused may already have been courted by, or recently copulated with, another male. In one experiment, male doves were paired with females who were either sexually eager or coy. The males courted the coy females, but responded aggressively to the "too eager" ones (Trivers, 1985: 265).
One way to help to ensure paternity is to guard one's mate from the sexual advances of other males -- this is termed "mate guarding." It is often essential because males will attempt to copulate with a female regardless of whether she is mated or not. In one study, male birds were temporarily removed from their territory. Their mates were indeed "hit on" by neighboring males (Kempenaers, Verheyen, & Dhondt, 1995). Similar male harassment has been observed in mice (Gubernik & Nordby, 1993). In a species of wasps, females who have recently copulated are receptive for a short time thereafter to the courtship of a second male. Not to be out-done, her first mate guards his investment by engaging in "female mimicry" to divert the attentions of a second male suitor (Field & Keller, 1993). This is termed "post-copulatory mate guarding."
Males of many species of birds follow their mates everywhere before egg laying to ward off other males. The male almost never allows her out of his sight (Birkhead, Atkin, & Molter, 1987). This is clearly mate guarding behavior because it occurs only during the time when the female is fertile -- the few days before egg-laying (Beecher & Beecher, 1979; Pinxten & Eens, 1997). In western bluebirds, females were followed with increasing intensity as the distance between the nearest neighbor was reduced and the threat of extra-pair copulation increased (Dickinson and Leonard, 1996). While engaging in mate guarding, male baboons travel shorter distances during foraging, and consequently have decreased caloric consumption (Alberts, Altmann, & Wilson, 1996). In evolutionary terms, the payoff in increased paternity assurance apparently balances the nutritional energy deficit.
Mate guarding in primates is also visible in the form of consortships, such as in resus maquaques (Carpenter, 1942). The male attempts to court a female during her fertile period by developing rapport with her, then he exhibits post-conception possessiveness. Tutin (1979) observed unique courthship in chimpanzees, which can last anywhere from hours to 28 days. The male starts by remaining close to a particular female and grooming her until enough of her sub-group is gone so he can lead her to private area. In following the male quietly, the female is complying with the male’s attempts to court her. However, should the female respond to other males’ calls or vocalize on her own, the interaction will end without results. Van Noordwijk (1985) adds that sometimes the females are the initiators, inviting the males to consort and never travelling far unless the male follows.
Unattractive and lower status males should have even greater concerns about the possibility of being cuckolded. Their mates are more likely to be receptive to invitations for EPCs (Hasselquist, Bensch, & von-Schantz, 1996; Kempenaers, Verheyen, Van-den-Broeck & Burke, 1992). Males of a species of bird, appropriately called "bluethroats," had their beautiful blue throats painted black by experimenters. Now, since they were no longer as attractive as the normal blue-throated males, they had more difficulty attracting a mate. And when they did, they guarded her more closely (Johnsen & Lifjeld, 1995). Amount of mate guarding thus appears to be a facultative adaptation, dependent on the attractiveness of the male, and, other variables as well -- for example, the fertility of the female (Miyashita, 1994).
Males who use mate guarding as a strategy for reproductive success allocate less energy to sperm production, therefore, producing four times less sperm than a male who depends on stealing or sneaking females as a reproduction strategy (Alonzo and Warner, 2000). As the risk of competition increased for the guarded Mediterranean Wrasse females, mate-guarding males amplified their mate guarding behavior rather than increasing their sperm production (Alonzo and Warner, 2000).
Another method to increase paternity assurance is sequestering -- removing the female to a place isolated from other males. On finding a receptive female, male wasps immediately remove her from the place where she is advertising her presence with pheromones (Alcock, 1981). Chimpanzee males also attempt to remove estrous females to a place hidden from male competitors (Packer, 1979). Females may also be sequestered using acoustical guarding as the means. In studies of vocal duets in the bay wren, it was predicted that a male is attracted to female songs to establish a duet and thereby, guard his female from establishing a song with any other male (Levin, 1996).
Using a combination of these strategies, males of a non-migratory duck species, the white-cheeked pintail, were observed vigorously defending their mates from other males that were attempting forced extra-pair copulations with their mates (Sorenson, 1994). The males “protected” their females by escorting them to their nests and by defending their own territory from other males. In addition, a male would copulate with his mate immediately after she was subjected to forced extra-pair copulation with another male to ensure his sperm would compete with another male’s sperm and to increase his likelihood of paternity (Sorenson, 1994). As seen in the red deer in Donana that depend on a “resource-defense system,” the success of a large male often depends largely on the location of his territory and his access to receptive females (Carranza, 1995).
Another direct way to insure paternity is simply to take the female's eggs from her, and guard the eggs instead of the female. As we learned in Chapter 4, this is the strategy of male sea horses.
Finally, males may actually resort to harming or injuring a female to prevent her from remating with another male after him. The evolution of genital barbs and spines and the transfer of dose-dependent toxins to a female during copulation may serves as a means for a male to guard a female and prevent or delay her from remating (Johnstone & Keller, 2000). A female who was injured by a male during copulation may choose to avoid future matings in order to protect herself from further pain or physical damage (Johnstone & Keller, 2000).
It is likely that many mammals experience an emotion similar to what we refer to as sexual jealousy. Jealousy is an emotional adaptation that functions as a mate guarding and retention mechanism. Although we cannot know exactly what emotions animals do experience, when males discover infidelity they often respond aggressively and/or abandon their mate. David Barash (1976) performed a clever experiment to incite "jealousy" in male mountain blackbirds. When the male was away from his mate, a model of a male blackbird was placed near the nest. When the male returned and saw the apparent "adultery" he aggressively attacked the model, attacked his mate, and, in one instance, even drove his mate away. When the experiment was repeated after the females had finished laying their eggs for the season, the response of the males was predictably less intense -- their assurance of paternity was no longer at risk.
Male paternity is also no longer at risk when a female is obviously pregnant. Only then can a male relax his mate guarding efforts. Male gorillas will tolerate a rival male copulating with his mate right in front of him -- as long as she is obviously pregnant.
If males are unsuccessful in preventing other males from mating, they have a few remaining tactics to use. In many mammalian species, as long as females are lactating, they cease ovulation. For the males of some species, the wait is too long for a female to wean her infants fathered by another male.
However, in many mammalian species, if females lose their nursing offspring, they will soon become sexually receptive again. You may guess what may evolve: male infanticide (the killing of infants) -- designed to re-start female ovulation.
Having lost their nursing infants, the females come into estrous again. They apparently do not hold grudges long -- they often mate with the murderer of their offspring soon after the bloodshed (Hausfater & Hrdy, 1984). Sugiyama (1967) first studied presumed infanticides in Hanuman langurs in western
Recent studies suggest that the evolutionary pressures on land that encourage infanticide may not be that different than pressures in the marine environment. Increased findings of dead, badly bruised and beaten bottlenose dolphins under the age of one year suggest infanticide may be occurring in this seemingly peaceful species (Milius, 1998). By killing a calf with uncertain paternity, a male bottlenose dolphin can cause a female to become receptive much more quickly than if he waited the two years necessary for the mother-calf pair to split. As predicted, observed cases of bottlenose dolphins showed females becoming fertile within 1 to 2 weeks of losing an infant (Milius, 1998).
Hrdy (1974, 1977) has extended the sexual-selection hypothesis to include these examples of male inflicted infanticide. The sexual-selection hypothesis suggests that a male should only kill infants sired by other males, that females who lose infants by infanticide will become fertile sooner, and that the murderous male should sire the female’s next offspring.
Male infanticide is often associated with polygynous mating systems, especially after a take-over by either a male outsider, or by a subordinate male from within the group who has not yet mated with any of the females. Once the females have provided him with his own offspring, the infanticidal male generally behaves tolerantly, even affectionately, to the infants.
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Insert Figure # here
Photo of infanticide.
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Sperm plugs
In several species, males have evolved some exotic forms of mate guarding. One way to guard your mate is to give her a chastity belt. Among some insect species, as well as in snakes, rats and guinea pigs, semen has a coagulation substance that causes the formation of a "mating plug" that plugs up the female reproductive tract. The plug not only helps to retain the male's sperm in the female reproductive tract, it prevents other males from copulating with her. In some species of mosquitoes, house flies, and butterflies, males have a substance in their semen that causes females to be less receptive to other males (Halliday, 1980). Male fruit flies produce chemicals that not only dampen female sexual libido, but also kill any rival sperm as well (Rice, 1996).
A rather radical option is simply to leave your genitals behind in the female reproductive tract as mating plug, as do the males of one species of fly (Parker, 1970). Or, plugs (without sperm) can be used to plug up the reproductive tract of other males -- as some male worms do to sterilize their competitors (Abele & Gilchrist, 1977).
In the great majority of vertebrate species, males are poor fathers. In many, they neither provision nor protect their offspring. Male parental investment is widespread in birds, and in some mammalian species, particularly rodents, carnivores and some primates (Clutton-Brock, 1991). As we have learned previously, the life history strategy of males generally apportions more investment to mating than to parenting. When males do parent, it is often because they must -- otherwise their reproductive success would diminish. For example, male birds are obligated to invest parentally -- if they did not, many (or all) of their offspring may not survive. Several studies have shown that when experimenters removed the father in mated bird pairs, his absence generally resulted in decreased survival and growth rates of the chicks (Mock & Fujioka, 1990; for a general review, see Clutton-Brock, 1991).
Male parental investment generally is dependent on two factors: (a) the ability of males to provision and/or protect their offspring, and (b) a high degree of paternity assurance. For example, in some species, males cannot offer food to their offspring because it is so dispersed and difficult to transport (grass, for example, among grazing species). In such cases it is not that males refuse to invest parentally -- they simply cannot.
In contrast, male social carnivores can provide their offspring with a highly compact and protein dense food, meat -- and they often do. Males should adjust their expenditure of parental investment as a function of their probability of paternity -- the higher the paternity assurance, the greater the likelihood of investment. When male investment is likely to be costly, males should be particularly demanding about the sexual fidelity of their mates (Daly & Wilson, 1987). Male swallows, for example, have been found to reduce their parental investment according to cues that indicate the likelihood that they have been cuckolded (Moller, 1988).
Even with high levels of paternity assurance, males may redirect their parental effort to mating effort should such opportunities arise. If new females arrive in their territories, male red-winged blackbirds will defer their parental care in favor of renewed mating effort (Muldal, Moffatt & Robertson, 1986). When experimenters made certain zebra finch males more attractive to females by using colored legbands, the males reduced their parental investment. Conversely, those who were given "unattractively colored" legbands increased their parenting effort (Burley, 1981, 1988). In another study, experimenters were able to increase the rate at which males deserted their offspring as a function of the sex ratio -- when more females were available for mating, male abandonment of offspring increased (Keenleyside, 1983).
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Insert Figure # about here
Percentage of males deserting
offspring as a function of the sex ratio.
(After Kennleyside, 1983)
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There are very few species where both parents invest equally. However, males may invest in indirect ways that may not immediately be perceived as parental investment. Males are more often involved in territorial defense, which includes the defense of eggs and offspring (Breitwisch, 1988). This would be a burden that would otherw